Evolution of Monogamy
The evolution of monogamy refers to the natural history of mating systems in which species reproduce by forming pairs to raise offspring. Animals The evolution of mating systems in animals has received an enormous amount of attention from biologists. It would take a book, or perhaps even several books, to thoroughly review everything biologists have learned about the evolution of animal mating systems. This section briefly reviews three main findings about the evolution of monogamy in animals. Types of Monogamy Biologists now have solid evidence that monogamous pairs of animals are not always sexually exclusive. Many animals that form pairs to mate and raise offspring regularly engage in sexual activities with extra-pair partners Ågren, G., Zhou, Q. & Zhong, W. (1989). Ecology and social behaviour of Mongolian gerbils Meriones unguiculatus, at Xiliuhot, Inner Mongolia, China. Animal Behaviour, 37, 11-27. Barash, D.P. (1981). Mate guarding and gallivanting by male hoary marmots (Marmota caligata). Behavioral Ecology and Sociobiology, 9, 187-193. Birkhead, T.R. & Møller, A.P. (1995). Extra-pair copulations and extra-pair paternity in birds. Animal Behaviour, 49, 843-848. Birkhead, T.R. & Møller, A.P. (1996). Monogamy and sperm competition in birds. In J. M. Black (Ed.), Partnerships in Birds: The Study of Monogamy (pp. 323-343). Oxford: Oxford University Press. Foltz, D.W. (1981). Genetic evidence for long-term monogamy in a small rodent, Peromyscus polionotus. American Naturalist, 117, 665-675. Gursky, S.L. (2000). Sociality in the spectral tarsier, Tarsius spectrum. American Journal of Primatology, 51, 89-101. Hasselquist, D. S. & Sherman, P.W. (2001). Social mating systems and extra pair fertilizations in passerine birds. Behavioral Ecology, 12, 457-466. Hubrecht, R.C. (1985). Home range size and use and territorial behavior in the common marmoset, Callithrix jacchus jacchus, at the Tapacura Field Station, Recife, Brazil. International Journal of Primatology, 6, 533-550. Mason, W.A. (1966). Social organization of the South American monkey, Callicebus moloch: a preliminary report. Tulane Studies in Zoology, 13, 23-28. McKinney, F., Derrickson, S.R., & Mineau, P. (1983). Forced copulation in waterfowl. Behaviour, 86, 250-294. Reichard, U. (1995). Extra-pair Copulations in a Monogamous Gibbon (Hylobates lar). Ethology, 100, 99-112. Reichard, U.H. (2002). Monogamy—A variable relationship. Max Planck Research, 3, 62-67. Richardson, P.R.K. (1987). Aardwolf mating system: overt cuckoldry in an apparently monogamous mammal. South African Journal of Science, 83, 405- 412. Welsh, D. & Sedinger, J.S. (1990). Extra-Pair copulations in Black Brant. The Condor, 92, 242-244. Owens, I.P.F. & Hartley, I.R. (1998). Sexual dimorphism in birds: why are there so many different forms of dimorphism? Proceedings of the Royal Society, London, B265, 397–407. Solomon, N.G., Keane, B., Knoch, L.R., & Hogan, P.J. (2004). Multiple paternity in socially monogamous prairie voles (Microtus ochrogaster). Canadian Journal of Zoology, 82, 1667-1671. These discoveries have led biologists to adopt new ways of talking about monogamy: "Social monogamy refers to a male and female's social living arrangement (e.g., shared use of a territory, behaviour indicative of a social pair, and/or proximity between a male and female) without inferring any sexual interactions or reproductive patterns. In humans, social monogamy equals monogamous marriage. Sexual monogamy is defined as an exclusive sexual relationship between a female and a male based on observations of sexual interactions. Finally, the term genetic monogamy is used when DNA analyses can confirm that a female-male pair reproduce exclusively with each other. A combination of terms indicates examples where levels of relationships coincide, e.g., sociosexual and sociogenetic monogamy describe corresponding social and sexual, and social and genetic monogamous relationships, respectively." (Reichard, 2003, page 4) Reichard, U.H. (2003). Monogamy: Past and present. In U.H. Reichard and C. Boesch (Eds.), Monogamy: Mating strategies and partnerships in birds, humans, and other mammals (pp.3-25).Cambridge: Cambridge University Press. Whatever makes a pair of animals socially monogamous does not necessarily make them sexually or genetically monogamous. Social monogamy, sexual monogamy, and genetic monogamy can occur in different combinations. Incidence of Monogamy Biologists agree that social monogamy is rare in the animal kingdom. The percentage of monogamous species is greater in some taxa than in others. Biologists estimate up to 90 percent of avian species are socially monogamous. Lack, D. (1968). Ecological Adaptations for Breeding in Birds. London: Methuen.Moller, A.P. (1986). Mating systems among European passerines: a review. Ibis, 7, 234-250. In contrast, biologists estimate only 3 percent of mammalian species are socially monogamous, although up to 15 percent of primate species are monogamous.Reichard, U.H. (2002). Monogamy—A variable relationship. Max Planck Research, 3, 62-67. Of course, sexual monogamy and genetic monogamy are even more rare than social monogamy, since so many socially monogamous species are not sexually monogamous. Gowaty has estimated that, out of 180 different species of socially monogamous songbirds, only 10 percent are sexually monogamous.Research conducted by Patricia Adair Gowaty. Reported by Morell, V. (1998). Evolution of sex: A new look at monogamy. Science, 281, 1982-1983. Causes of Monogamy Socially monogamous species are scattered throughout the animal kingdom. A few insects are socially monogamous; a few fish are socially monogamous; a lot of birds are socially monogamous; and a few mammals are socially monogamous. These species did not inherit social monogamy from a common ancestor. Instead, social monogamy has evolved independently in different species. Some factors that contribute to the evolution of social monogamy include: * resources available in the surrounding environment Harding, J.A., Almany, G.R., Houck, L.D., & Hixon, M.A. (2003). Experimental analysis of monogamy in the Caribbean cleaner goby, Gobiosoma evelynae. Animal Behaviour, 65, 865–874. * geographic distribution of mates Komers, P.E. & Brotherton, P.N.M. (1997) Female space use is the best predictor of monogamy in mammals. Proceedings of the Royal Society of London, Series B, 264, 1261-1270. * incidence of parasites and sexually transmitted diseases Altizer, S., et al. (2003). Social organization and parasite risk in mammals: Integrating theory and empirical studies. Annual Review of Ecology, Evolution, and Systematics, 34, 517-547. * amount of parental care given to offspring Lack, D. (1968). Ecological Adaptations for Breeding in Birds. London: Methuen. * mate guarding behaviorsMathews, L.M. (2003). Tests of the mate- guarding hypothesis for social monogamy: male snapping shrimp prefer to associate with high-value females. Behavioral Ecology, 14, 63-67. * infanticide Palombit, R. A. (1999). Infanticide and the evolution of pair bonds in nonhuman primates. Evolutionary Anthropology: Issues, News, and Reviews, 7, 117-129. * length of breeding season Weatherhead, P.J. (1979). Ecological correlates of monogamy in tundra-breeding Savannah Sparrows. The Auk, 96, 391-401. * chemical mechanisms of bonding in the brain Young, L.J., Wang, Z., & Insel, T.R. (1998). Neuroendocrine bases of monogamy. Trends in Neuroscience, 21, 71-75. This list is not complete. Other factors may also contribute to the evolution of social monogamy. Moreover, different sets of factors may explain the evolution of social monogamy in different species. There is no one-size-fits-all explanation of why different species evolved monogamous mating systems. Humans The evolution of monogamy in humans is a particularly difficult problem. Human behaviors do not fossilize, so there is no way to know for certain whether or not human ancestors were monogamous. Researchers are forced to draw inferences from characteristics believed to be related to mating systems (e.g., sexual dimorphism and testes size). These inferences are often weakened by questionable assumptions and conflicting data. The evolution of monogamy in humans remains largely a matter of speculation and educated guesses. Closest Genetic Relatives DNA evidence has established the evolutionary relationships between humans, chimpanzees, bonobos, and gorillas. All four of these species once shared a common ancestor. The first split between the species occurred when gorillas diverged from the common ancestor of humans, bonobos, and chimpanzees. The next split occurred when humans diverged from the common ancestor of bonobos and chimpanzees. The split between bonobos and chimpanzees occurred most recently. This makes bonobos and chimpanzees the closest genetic relatives to humans. (If you'd like to learn more about the evolutionary family tree, see the Wikipedia articles on Human Evolution and Apes.) What can the mating systems of close genetic relatives reveal about the evolution of monogamy in humans? One answer to this question is that, because humans are genetically closest to bonobos and chimpanzees, humans may still have genes for promiscuity. Another answer to the question is that, because humans are most closely related to bonobos and chimpanzees, the promiscuity of bonobos and chimpanzees serves as the best model for mating in the early ancestors of humans. Both answers suggest human ancestors may have been promiscuous rather than monogamous. Unfortunately, both of these answers assume millions of years of evolution have not changed the mating systems of bonobos and chimpanzees. This assumption is strongly challenged by fossil evidence. Fossils of Sahelanthropus suggest the common ancestor of humans, bonobos and chimpanzees was not like a modern bonobo or a modern chimpanzee. "Most surprising of all may be what Sahelanthropus reveals about the last common ancestor of humans and chimpanzees. Paleoanthropologists have typically imagined that that creature resembled a chimp in having, among other things, a strongly projecting lower face, thinly enameled molars and large canines. Yet Sahelanthropus, for all its generally apelike traits, has only a moderately prognathic face, relatively thick enamel, small canines and a brow ridge larger than that of any living ape. 'If Sahelanthropus shows us anything, it shows us that the last common ancestor was not a chimpanzee,' Berkeley’s White remarks. 'But why should we have expected otherwise?' Chimpanzees have had just as much time to evolve as humans have had, he points out, and they have become highly specialized, fruit-eating apes." (Wong, 2003, page 61) Wong, K. (2003). An ancestor to call our own. Scientific American, 288, 54-63. Fossils of Australopithecus suggest early human ancestors were highly sexually dimorphic, a characteristic not shared by modern bonobos and chimpanzees. A high amount of sexual dimorphism sometimes indicates a polygamous mating system. Owens, I.P.F. & Hartley, I.R. (1998). Sexual dimorphism in birds: why are there so many different forms of dimorphism? Proceedings of the Royal Society of London B, 265, 397-407. Frayer, D.W. & Wolpoff, M.H. (1985). Sexual dimorphism. Annual Review of Anthropology, 14, 429-473. Geary, D.C., & Flinn, M.V. (2001). Evolution of human parental behavior and the human family. Parenting: Science and Practice, 1, 5-61. Sexual dimorphism in Australopithecus raises questions about the validity of comparing modern bonobos and chimpanzees to human ancestors. Bonobos and chimpanzees have undergone millions of years of evolution since they split from the common ancestor with humans. Sexual promiscuity in bonobos and chimpanzees may have evolved after the split from the common ancestor with humans. In that case, humans would not share the genes for promiscuity, and modern bonobos and chimpanzees would not be good models for sexual behavior in early human ancestors. It is simply not possible to draw conclusions about the evolution of monogamy in humans by studying the mating systems of modern bonobos and chimpanzees. Sexual Dimorphism Sexual dimorphism refers to differences in body characteristics between males and females. A frequently studied type of sexual dimorphism is body size. Males typically have larger bodies than females. In some species, however, females have larger bodies than males. Sexual dimorphism in body size has been linked to mating behavior. Owens, I.P.F. & Hartley, I.R. (1998). Sexual dimorphism in birds: why are there so many different forms of dimorphism? Proceedings of the Royal Society of London B, 265, 397-407. Frayer, D.W. & Wolpoff, M.H. (1985). Sexual dimorphism. Annual Review of Anthropology, 14, 429-473. Geary, D.C., & Flinn, M.V. (2001). Evolution of human parental behavior and the human family. Parenting: Science and Practice, 1, 5-61. Dunn, P.O., Whittingham, L.A., & Pitcher, T.E. (2001). Mating systems, sperm competition, and the evolution of sexual dimorphism in birds. Evolution, 55, 161–175. In polygamous species, males compete for control over sexual access to females. Large males have an advantage in the competition for access to females, and they consequently pass their genes along to a greater number of offspring. This eventually leads to large differences in body size between males and females. Polygamous males are often 1.5 to 2.0 times larger in size than females. In monogamous species, on the other hand, males and females have more equal access to mates, so there is little or no sexual dimorphism in body size. Some researchers have attempted to infer the evolution of human mating systems from the evolution of sexual dimorphism. Several studies have reported a large amount of sexual dimorphism in Australopithecus, an evolutionary ancestor of human beings that lived between 2 and 4 million years ago. Frayer, D.W. & Wolpoff, M.H. (1985). Sexual dimorphism. Annual Review of Anthropology, 14, 429-473. Geary, D.C., & Flinn, M.V. (2001). Evolution of human parental behavior and the human family. Parenting: Science and Practice, 1, 5-61. Flinn, M.V. & Ward, C.V. (2004). Ontogeny and Evolution of the Social Child. In: Origins of the social mind: Evolutionary psychology and child development, B. Ellis & D. Bjorklund (Eds.), chapter 2, pp. 19-44. London: Guilford Press. Lockwood, C.A., Richmond, B.G., Jungers, W.L., & Kimbel, W.H. (1996). Randomization procedures and sexual dimorphism in Australopithecus afarensis. Journal of Human Evolution, 31, 537-548. These studies raise the possibility that Australopithecus had a polygamous mating system. Sexual dimorphism then began to decrease. Studies suggest sexual dimorphism reached modern human levels around the time of Homo Erectus 0.5 to 2 million years ago. Frayer, D.W. & Wolpoff, M.H. (1985). Sexual dimorphism. Annual Review of Anthropology, 14, 429-473. Geary, D.C., & Flinn, M.V. (2001). Evolution of human parental behavior and the human family. Parenting: Science and Practice, 1, 5-61. Flinn, M.V. & Ward, C.V. (2004). Ontogeny and Evolution of the Social Child. In: Origins of the social mind: Evolutionary psychology and child development, B. Ellis & D. Bjorklund (Eds.), chapter 2, pp. 19-44. London: Guilford Press. Arsuaga, J.L., Carretero, J.M., Lorenzo, C., Gracia, A., Martínez, I., Bermúdez de Castro, J.M., & Carbonell, E. (1997). Size variation in Middle Pleistocene humans. Science, 277, 1086-1088. This line of reasoning suggests human ancestors started out polygamous and began the transition to monogamy somewhere between 0.5 million and 2 million years ago. Attempts to infer the evolution of monogamy based on sexual dimorphism remain controversial for three reasons: * The skeletal remains of Australopithecus are quite fragmentary. This makes it difficult to identify the sex of the fossils. Researchers sometimes identify the sex of the fossils by their size, which, of course, can exaggerate findings of sexual dimorphism. * Recent studies using new methods of measurement suggest Australopithecus had the same amount of sexual dimorphism as modern humans. Reno, P.L., Meindl, R.S., McCollum, M.A., & Lovejoy, C.O. (2003). Sexual dimorphism in Australopithecus afarensis was similar to that of modern humans. Proceedings of the National Academy of Sciences, 100, 9404-9409.Larsen, C.S. (2003). Equality for the sexes in human evolution? Early hominid sexual dimorphism and implications for mating systems and social behavior. Proceedings of the National Academy of Sciences, 100, 9103-9104. This raises questions about the amount of sexual dimorphism in Australopithecus. * Even if future studies clearly establish sexual dimorphism in Australopithecus, other studies have shown the relationship between sexual dimorphism and mating system is unreliable. Owens, I.P.F. & Hartley, I.R. (1998). Sexual dimorphism in birds: why are there so many different forms of dimorphism? Proceedings of the Royal Society, London, B265, 397–407. Frayer, D.W. & Wolpoff, M.H. (1985). Sexual dimorphism. Annual Review of Anthropology, 14, 429-473. Some polygamous species show little or no sexual dimorphism. Some monogamous species show a large amount of sexual dimorphism. Studies of sexual dimorphism raise the possibility that early human ancestors were polygamous rather than monogamous. But this line of research remains highly controversial. It may be that early human ancestors showed little sexual dimorphism, and it may be that sexual dimorphism in early human ancestors had no relationship to their mating systems. Testis Size The relative sizes of male testes often reflect mating systems. Pitcher, T.E., Dunn, P.O., & Whittingham, L.A. (2005). Sperm competition and the evolution of testes size in birds. Journal of Evolutionary Biology, 18, 557–567. Simmons, L.W., Firman, R.E.C., Rhodes, G., & Peters, M. (2004). Human sperm competition: testis size, sperm production and rates of extrapair copulations. Animal Behaviour, 68, 297-302. Dixson, A., & Anderson, M. (2001). Sexual selection and the comparative anatomy of reproduction in monkeys, apes, and human beings. Annual Review of Sex Research, 12, 121-144. Harcourt, A.H., Harvey, P.H., Larson, S.G., & Short, R.V. (1981). Testis weight, body weight and breeding system in primates. Nature, 293, 55-57. In species with promiscuous mating systems, where many males mate with many females, the testes tend to be relatively large. This appears to be the result of sperm competition. Males with large testes produce more sperm and thereby gain an advantage impregnating females. In polygynous species, where one male controls sexual access to females, the testes tend to be small. One male defends exclusive sexual access to a group of females and thereby eliminates sperm competition. Studies of primates, including humans, support the relationship between testis size and mating system. Dixson, A., & Anderson, M. (2001). Sexual selection and the comparative anatomy of reproduction in monkeys, apes, and human beings. Annual Review of Sex Research, 12, 121-144. Harcourt, A.H., Harvey, P.H., Larson, S.G., & Short, R.V. (1981). Testis weight, body weight and breeding system in primates. Nature, 293, 55-57. Chimpanzees, which have a promiscuous mating system, have large testes compared to other primates. Gorillas, which have a polygynous mating system, have smaller testes than other primates. Humans, which have a socially monogamous mating system, accompanied by moderate amounts of sexual non-monogamy, have moderately sized testes. The moderate amounts of sexual non-monogamy in humans may result in a low to moderate amount of sperm competition. Although testis size in humans is consistent with the modern pattern of social monogamy accompanied by moderate sexual non-monogamy, this fact reveals little about when the modern pattern evolved. Did Homo Erectus have testes similar in size to modern humans? What about Australopithecus? It is not possible to measure the size of testes in the fossil remains of human ancestors. This limits the usefulness of testis size in understanding the evolution of monogamy in humans. Cultural Evolution Culture has clearly increased the incidence of social monogamy. Many modern cultures have passed laws making social monogamy the only legal form of marriage. The passage of such laws in many cases reflects the spread of Christianity. However, in recent years, international organizations such as the United Nations and the African Union have started to promote social monogamy as a way to give women and men equal rights in marriage. The United Nations started to promote social monogamy as the preferred form of marriage in 1979 when the General Assembly adopted the Convention on the Elimination of All Forms of Discrimination Against Women, an international bill of rights for women that over 180 nations have agreed to implement. Article 16 of the Convention requires nations to give women and men equal rights in marriage. Polygamy is interpreted as inconsistent with Article 16 because it extends the right of multiple spouses to men but not to women. The United Nations has established the Committee on the Elimination of Discrimination against Women, or CEDAW, to monitor the progress of nations implementing the Convention. The United Nations is thus working through the Convention and CEDAW to promote women's equality by making monogamy the only legal form of marriage worldwide. The African Union has recently adopted the Protocol on the Rights of Women in Africa. While the protocol does not suggest making polygamous marriage illegal, article 6 of the protocol states that "monogamy is encouraged as the preferred form of marriage and that the rights of women in marriage and family, including in polygamous marital relationships are promoted and protected." Amnesty International, 2006. The Protocol on the Rights of Women in Africa: Strengthening the promotion and protection of women’s human rights in Africa. Retrieved May 29, 2006 from http://web.archive.org/web/20040626065311/http://web.amnesty.org/library/Index/ENGIOR630052004 .University of Minnesota Human Rights Library, 2006. Protocol to the African Charter on Human and Peoples' Rights on the Rights of Women in Africa. Retrieved May 29, 2006 from http://www1.umn.edu/humanrts/africa/protocol- women2003.html . The protocol entered into force November 25, 2005. Readers interested in the cultural evolution of monogamy may wish to visit the Wikipedia article on the history of human sexuality. References See also * Monogamy * Varieties of Monogamy * Incidence of Monogamy * Value of Monogamy * Psychology of Monogamy * Evolution of Monogamy Related Links * Evolution * Evolution of sex * Animal sexuality * Human Evolution * History of human sexuality Category:Marriage